Skip to main content
SpringerLink
Log in

Arachidonic acid is a chemoattractant for Dictyostelium discoideum cells

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Cyclic AMP (cAMP) is a natural chemoattractant of the social amoeba Dictyostelium discoideum. It is detected by cell surface cAMP receptors. Besides a signalling cascade involving phosphatidylinositol 3,4,5-trisphosphate (PIP3), Ca2+ signalling has been shown to have a major role in chemotaxis. Previously, we have shown that arachidonic acid (AA) induces an increase in the cytosolic Ca2+ concentration by causing the release of Ca2+ from intracellular stores and activating influx of extracellular Ca2+. Here we report that AA is a chemoattractant for D. discoideum cells differentiated for 8–9 h. Motility towards a glass capillary filled with an AA solution was dose-dependent and qualitatively comparable to cAMP-induced chemotaxis. Ca2+ played an important role in AA chemotaxis of wild-type Ax2 as ethyleneglycolbis(b-aminoethyl)-N,N,N′,N′-tetraacetic acid (EGTA) added to the extracellular buffer strongly inhibited motility. In the HM1049 mutant whose iplA gene encoding a putative Ins(1,4,5)P3-receptor had been knocked out, chemotaxis was only slightly affected by EGTA. Chemotaxis in the presence of extracellular Ca2+ was similar in both strains. Unlike cAMP, addition of AA to a cell suspension did not change cAMP or cGMP levels. A model for AA chemotaxis based on the findings in this and previous work is presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bumann J, Wurster B and Malchow D 1984 Attractant-induced changes and oscillations of the extracellular Ca2+ concentration in suspensions of differentiating Dictyostelium cells; J. Cell Biol. 98 173–178

    Article  CAS  Google Scholar 

  • Cameron A M, Steiner J P, Roskams A J, Ali S M, Ronnett G V and Snyder S H 1995 Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux; Cell 83 463–472

    Article  CAS  Google Scholar 

  • Chen L, Iijima M, Tang M, Landree M A, Huang Y E, Xiong Y, Iglesias P A and Devreotes P N 2007 PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis; Dev. Cell 12 603–614

    Article  CAS  Google Scholar 

  • Condeelis J 2001 How is actin polymerization nucleated in vivo?; Trends Cell Biol. 11 288–293

    Article  CAS  Google Scholar 

  • Davidoff F and Korn E D 1963a The biosynthesis of fatty acids in the cellular slime mold, Dictyostelium discoideum; J. Biol. Chem. 238 3210–3215

    CAS  PubMed  Google Scholar 

  • Davidoff E and Korn E D 1963b Fatty acid and phospholipid composition of the cellular slime mold, Dictyostelium discoideum. The occurrence of previously undescribed fatty acids; J. Biol. Chem. 238 3199–3209

    CAS  PubMed  Google Scholar 

  • Flaadt H, Jaworski E and Malchow D 1993a Evidence for two intracellular calcium pools in Dictyostelium: the cAMP-induced calcium influx is directed into a NBD-Cl-and 2,5-di-(tert-butyl)-1,4-hydroquinone-sensitive pool; J. Cell Sci. 105 1131–1135

    CAS  PubMed  Google Scholar 

  • Flaadt H, Jaworski E, Schlatterer C and Malchow D 1993b Cyclic AMP-induced and Ins(1,4,5)P3-induced Ca2+ fluxes in permeabilized cells of Dictyostelium discoideum — cGMP regulates Ca2+ entry across the plasma membrane; J. Cell Sci. 105 255–261

    CAS  Google Scholar 

  • Furukawa R, Maselli A, Thomson S A, Lim R W, Stokes J V and Fechheimer M 2003 Calcium regulation of actin crosslinking is important for function of the actin cytoskeleton in Dictyostelium; J. Cell Sci. 116 187–196

    Article  CAS  Google Scholar 

  • Gauthier M L and O’Day D H 2001 Detection of calmodulin-binding proteins and calmodulin-dependent phosphorylation linked to calmodulin-dependent chemotaxis to folic and cAMP in Dictyostelium; Cell Signal 13 575–584

    Article  CAS  Google Scholar 

  • Gerisch G and Hess B 1974 Cyclic-AMP-controlled oscillations in suspended Dictyostelium cells: Their relation to morphogenetic cell interactions; Proc. Natl. Acad. Sci. USA 71 2118–2122

    Article  CAS  Google Scholar 

  • Gerisch G and Malchow D 1976 Cyclic AMP receptors and the control of cell aggregation in Dictyostelium; Adv. Cycl. Nucl. Res. 7 49–68

    CAS  Google Scholar 

  • Gollnick F, Meyer R and Stockem W 1991 Visualization and measurement of calcium transients in Amoeba proteus by fura-2 fluorescence; Eur. J. Cell Biol. 55 262–271

    CAS  PubMed  Google Scholar 

  • Heid P J, Geiger J, Wessels D, Voss E and Soll D R 2005 Computer-assisted analysis of filopod formation and the role of myosin II heavy chain phosphorylation in Dictyostelium; J. Cell Sci. 118 2225–2237

    Article  CAS  Google Scholar 

  • Jalink K, Moolenaar W H and van Duijn B 1993 Lysophosphatidic acid is a chemoattractant for Dictyostelium discoideum amoebae; Proc. Natl. Acad. Sci. USA 90 1857–1861

    Article  CAS  Google Scholar 

  • Kessen U, Schaloske R, Aichem A and Mutzel R 1999 Ca2+/calmodulin-independent activation of calcineurin from Dictyostelium by unsaturated long chain fatty acids; J. Biol. Chem. 274 37821–37826

    Article  CAS  Google Scholar 

  • Kimmel A R and Firtel R A 2004 Breaking symmetries: regulation of Dictyostelium development through chemoattractant and morphogen signal-response; Curr. Opin. Genet. Dev. 14 540–549

    Article  CAS  Google Scholar 

  • Lusche D F, Bezares-Roder K, Happle K and Schlatterer C 2005a cAMP controls cytosolic Ca2+ levels in Dictyostelium discoideum; BMC Cell Biol. 6 12

    Article  Google Scholar 

  • Lusche D F, Kaneko H and Malchow D 2005b cGMP-phosphodiesterase antagonists inhibit Ca2+-influx in Dictyostelium discoideum and bovine cyclic-nucleotide-gated-channel; Eur. J. Pharmacol. 513 9–20

    Article  CAS  Google Scholar 

  • Lusche D F and Malchow D 2005 Developmental control of cAMP-induced Ca2+-influx by cGMP: influx is delayed and reduced in a cGMP-phosphodiesterase D deficient mutant of Dictyostelium discoideum; Cell Calcium 37 57–67

    Article  CAS  Google Scholar 

  • Ma L, Janetopoulos C, Yang L, Devreotes P N and Iglesias P A 2004 Two complementary, local excitation, global inhibition mechanisms acting in parallel can explain the chemoattractant-induced regulation of PI(3,4,5)P3 response in Dictyostelium cells; Biophys. J. 87 3764–3774

    Article  CAS  Google Scholar 

  • Malchow D, Bohme R and Gras U 1982 On the role of calcium in chemotaxis and oscillations of Dictyostelium cells; Biophys. Struct. Mech. 9 131–136

    Article  CAS  Google Scholar 

  • Manahan C L, Iglesias P A, Long Y and Devreotes P N 2004 Chemoattractant signaling in Dictyostelium discoideum; Annu. Rev. Cell. Dev. Biol. 20 223–253

    Article  CAS  Google Scholar 

  • Menz S, Bumann J, Jaworski E and Malchow D 1991 Mutant analysis suggests that cyclic GMP mediates the cyclic AMPinduced Ca2+ uptake in Dictyostelium; J. Cell Sci. 99 187–191

    CAS  PubMed  Google Scholar 

  • Mignen O, Thompson J L and Shuttleworth T J 2003a Ca2+ selectivity and fatty acid specificity of the noncapacitative, arachidonate-regulated Ca2+ (ARC) channels; J. Biol. Chem. 278 10174–10181

    Article  CAS  Google Scholar 

  • Mignen O, Thompson J L and Shuttleworth T J 2003b Calcineurin directs the reciprocal regulation of calcium entry pathways in nonexcitable cells; J. Biol. Chem. 278 40088–40096

    Article  CAS  Google Scholar 

  • Montell C and Devreotes P 2004 From protein dynamics to animal behavior: new insights into complex cell regulatory mechanisms; Curr. Opin. Cell Biol. 16 115–118

    Article  CAS  Google Scholar 

  • Newell P C 1995 Signal transduction and motility of Dictyostelium; Biosci. Rep. 15 445–462

    Article  CAS  Google Scholar 

  • Newell P C, Malchow D and Gross J D 1995 The role of calcium in aggregation and development of Dictyostelium; Experientia 51 1155–1165

    Article  CAS  Google Scholar 

  • Parent C A 2004 Making all the right moves: chemotaxis in neutrophils and Dictyostelium; Curr. Opin. Cell Biol. 16 4–13

    Article  CAS  Google Scholar 

  • Postma M, Bosgraaf L Loovers H M and Van Haastert P J 2004 Chemotaxis: signalling modules join hands at front and tail; EMBO Rep. 5 35–40

    Article  CAS  Google Scholar 

  • Schaloske R and Malchow D 1997 Mechanism of cAMP-induced Ca2+ influx in Dictyostelium: role of phospholipase A2; Biochem. J. 327 233–238

    Article  CAS  Google Scholar 

  • Schaloske R, Schlatterer C and Malchow D 2000 A xestospongin C-sensitive Ca2+ store is required for cAMP-induced Ca2+ influx and cAMP oscillations in Dictyostelium; J. Biol. Chem. 275 8404–8408

    Article  CAS  Google Scholar 

  • Schaloske R, Sonnemann J, Malchow D and Schlatterer C 1998 Fatty acids induce release of Ca2+ from acidosomal stores and activate capacitative Ca2+ entry in Dictyostelium discoideum; Biochem. J. 332 541–548

    Article  CAS  Google Scholar 

  • Schaloske R H, Lusche D F, Bezares-Roder K, Happle K, Malchow D and Schlatterer C 2005 Ca2+ regulation in the absence of the iplA gene product in Dictyostelium discoideum; BMC Cell Biol. 6 13

    Article  Google Scholar 

  • Schlatterer C, Buravkov S, Zierold K and Knoll G 1994a Calcium-sequestering organelles of Dictyostelium discoideum: Changes in element content during early development as measured by electron probe X-ray microanalysis; Cell Calcium 16 101–111

    Article  CAS  Google Scholar 

  • Schlatterer C, Gollnick F, Schmidt E, Meyer R and Knoll G 1994b Challenge with high concentrations of cyclic AMP induces transient changes in the cytosolic free calcium concentration in Dictyostelium discoideum; J. Cell Sci. 107 2107–2115

    CAS  PubMed  Google Scholar 

  • Schlatterer C, Happle K, Lusche D F and Sonnemann J 2004 Cytosolic [Ca2+] transients in Dictyostelium discoideum depend on the filling state of internal stores and on an active sarco/endoplasmic reticulum calcium ATPase (SERCA) Ca2+ pump; J. Biol. Chem. 279 18407–18414

    Article  CAS  Google Scholar 

  • Schlatterer C and Malchow D 1993 Intracellular guanosine-5′-0-(3-thiotriphosphate) blocks chemotactic motility of Dictyostelium discoideum amoebae; Cell Motil. Cytoskel. 25 298–307

    Article  CAS  Google Scholar 

  • Schlatterer C and Schaloske R 1996 Calmidazolium leads to an increase in the cytosolic Ca2+ concentration in Dictyostelium discoideum by induction of Ca2+ release from intracellular stores and influx of extracellular Ca2+; Biochem. J. 313 661–667

    Article  CAS  Google Scholar 

  • Shuttleworth T J 2004 Receptor-activated calcium entry channels— who does what, and when?; Sci. STKE 2004 pe40

    Article  Google Scholar 

  • Shuttleworth T J, Thompson J L and Mignen O 2004 ARC channels: a novel pathway for receptor-activated calcium entry; Physiology (Bethesda) 19 355–361

    CAS  Google Scholar 

  • Sneyd J, Tsaneva-Atanasova K, Yule D I, Thompson J L and Shuttleworth T J 2004 Control of calcium oscillations by membrane fluxes; Proc. Natl. Acad. Sci. USA 101 392–1396

    Article  Google Scholar 

  • Soll D R, Wessels D, Heid P J and Zhang H 2002 A contextual framework for characterizing motility and chemotaxis mutants in Dictyostelium discoideum; J. Muscle Res. Cell Motil. 23 659–672

    Article  CAS  Google Scholar 

  • Sonnemann J, Knoll G and Schlatterer C 1997 cAMP-induced changes in the cytosolic free Ca2+ concentration in Dictyostelium discoideum are light sensitive; Cell Calcium 22 65–74

    Article  CAS  Google Scholar 

  • Stepanovic V, Wessels D, Daniels K, Loomis W F and Soll D R 2005 Intracellular role of adenylyl cyclase in regulation of lateral pseudopod formation during Dictyostelium chemotaxis; Eukaryot. Cell 4 775–786

    Article  CAS  Google Scholar 

  • Traynor D, Milne J L S, Insall R H and Kay R R 2000 Ca2+ signalling is not required for chemotaxis in Dictyostelium; EMBO J. 19 4846–4854

    Article  CAS  Google Scholar 

  • Unterweger N and Schlatterer C 1995 Introduction of calcium buffers into the cytosol of Dictyostelium discoideum amoebae alters cell morphology and inhibits chemotaxis; Cell Calcium 17 97–110

    Article  CAS  Google Scholar 

  • Van Haastert P J and Devreotes P N 2004 Chemotaxis: signalling the way forward; Nat. Rev. Mol. Cell Biol. 5 626–634

    Article  Google Scholar 

  • Van Haastert P J, Keizer-Gunnink I and Kortholt A 2007 Essential role of PI3-kinase and phospholipase A2 in Dictyostelium discoideum chemotaxis; J. Cell Biol. 177 809–816

    Article  Google Scholar 

  • Veltman D M, de Boer J S and van Haastert P J M 2003 Chemoattractant-stimulated calcium influx in Dictyostelium discoideum does not depend on cGMP; Biochim. Biophys. Acta 1623 129–134

    Article  CAS  Google Scholar 

  • Weeks G and Herring F G 1980 The lipid composition and membrane fluidity of Dictyostelium discoideum plasma membranes at various stages during differentiation; J. Lipid Res. 21 681–686

    CAS  PubMed  Google Scholar 

  • Wessels D, Brincks R, Kuhl S, Stepanovic V, Daniels K J, Weeks G, Lim C J, Spiegelman G, Fuller D, Iranfar N, Loomis W F and Soll D R 2004 RasC plays a role in transduction of temporal gradient information in the cyclic-AMP wave of Dictyostelium discoideum; Eukaryot. Cell 3 646–662

    Article  CAS  Google Scholar 

  • Wessels D J, Zhang H, Reynolds J, Daniels K, Heid P, Lu S L, Kuspa A, Shaulsky G, Loomis W F and Soll D R 2000 The internal phosphodiesterase RegA is essential for the suppression of lateral pseudopods during Dictyostelium chemotaxis; Mol. Biol. Cell 11 2803–2820

    Article  CAS  Google Scholar 

  • Williams H P and Harwood A J 2003 Cell polarity and Dictyostelium development; Curr. Opin. Microbiol. 6 621–627

    Article  CAS  Google Scholar 

  • Wurster B, Schubiger K, Wick U and Gerisch G 1977 Cyclic GMP in Dictyostelium discoideum: oscillations and pulses in response to folic acid and cyclic AMP signals; FEBS Lett. 76 141–144

    Article  CAS  Google Scholar 

  • Yumura S, Furuya K and Takeuchi I 1996 Intracellular free calcium responses during chemotaxis of Dictyostelium cells; J. Cell Sci. 109 2673–2678

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA, 92093-0601, USA

    Ralph H. Schaloske

  2. Pharmaceutical Institute, Universty of Tuebingen, Morgenstelle 8, 72076, Tuebingen, Germany

    Dagmar Blaesius

  3. Department of Biology, University of Konstanz, Universitaetsstr.10, 78457, Konstanz, Germany

    Christina Schlatterer

  4. W M Keck Dynamic Image Analysis Facility, Department of Biological Sciences, The University of Iowa, Iowa City, IA, 52242, USA

    Daniel F. Lusche

Authors
  1. Ralph H. Schaloske
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dagmar Blaesius
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christina Schlatterer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel F. Lusche
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel F. Lusche.

Additional information

These authors contributed equally to this work.

This work was carried out at the University of Konstanz, Department of Biology, Universitaetstr.10, 78457 Konstanz, Germany.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schaloske, R.H., Blaesius, D., Schlatterer, C. et al. Arachidonic acid is a chemoattractant for Dictyostelium discoideum cells. J. Biosci. 32 (Suppl 3), 1281–1289 (2007). https://doi.org/10.1007/s12038-007-0137-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12038-007-0137-6

Keywords

Search

Navigation